Do scavengers prevent or promote disease transmission? The effect of invertebrate scavenging on Ranavirus transmission

Abstract

Host–parasite interactions are shaped by the broader web of community interactions, from interspecific competition to predator–prey dynamics. Heterospecific scavengers might also affect parasite transmission from infectious carcasses, which can be an important source of infections for some wildlife diseases. A robust scavenger community can quickly remove carcasses and tissue and thus prevent secondary transmission by necrophagy or contact with infectious carcasses. Alternatively, by spreading infectious particles and tissues throughout the environment, scavengers may increase rates of casual contact with pathogens and thus overall transmission. However, there has been little empirical consideration of the contrasting roles that scavengers might play in infectious disease dynamics. We carried out a series of studies to determine the efficiency with which scavenging invertebrates remove carcasses of Long‐toed Salamander (Ambystoma macrodactylum) larvae and their role in the transmission of frog virus 3 (Genus: Ranavirus, Family: Iridoviridae) from carcasses. We then estimated the functional response of one efficient invertebrate scavenger (Family: Dytiscidae) to increasing carcass densities in field conditions in order to determine the capacity of scavenging invertebrates to consume large amounts of carcass tissue, as may be present at high prevalence sites. We found that removal of infectious carcasses by scavengers strongly reduced transmission to naïve larvae. Scavengers were as effective at reducing transmission from a carcass as a physical barrier preventing contact with the carcass. There was little evidence that scavenging released sufficient infectious tissues into the water column to rival direct contact as a route of infection. Moreover, while scavenging rates saturated at increasing carcass densities, consistent with a type II functional response, there were sufficient densities of dytiscid larvae, not to mention other scavenging invertebrates, in a surveyed pond to theoretically prevent transmission from carcasses. Our results suggest that at least in systems in which conspecific necrophagy is common, the scavenger community can play an important role in reducing transmission. A plain language summary is available for this article.

Predator and scavenger movements among and within endangered seabird colonies: Opportunities for pathogen spread

“…However, we do not recommend culling native terrestrial predators as there are growing evidences that scavenging contribute in disease controls (e.g. Le Sage, Towey, & Brunner, ) and the culling of a native species would raise strong ethical issues. In the case of avian cholera on Amsterdam Island, an autogenous vaccine has proven efficient to protect yellow‐nosed albatross nestlings (Bourret et al, ), but whether it blocks transmission remains to be investigated.…”

Genetic Strain Diversity of Multi-Host RNA Viruses that Infect a Wide Range of Pollinators and Associates is Shaped by Geographic Origins

“…Nevertheless, feeding experiments have shown that scavenger species like the ant Myrmica rubra are found positive for the negative strand of DWV for up to 13 weeks after consuming infected honey bees [14], which indicates that DWV actively infects ants. Whether honey bee scavengers are able to spread viruses without becoming infected themselves [79] or aid in reducing virus transmission by removing infectious carcasses [80] remains to be tested. The detection of negative strand intermediates is an essential step in identifying host species, but only controlled infection experiments allow determination of the virus dynamics in these hosts and the potential for disease emergence.…”

Carcass Scavenging Relaxes Chemical-Driven Female Interference Competition

“…Animal death due to infection and disease can produce considerable variation in the quality of available carcasses (Devault et al 2003;Sage et al 2019). Infected carcasses may have lower nutritional value due to microbial overgrowth (Devault et al 2003) and increased infection risk (Sage et al 2019), reducing the net fitness effects of scavenging. To test this possibility, we directly .…”

“…Although these infected carcasses still serve as an essential nutrient source, overall quality might be poor due to excessive microbial growth (Milutinović et al 2015). However, these carcasses might not only reduce the net benefits of scavenging, but they can also increase the risk of disease transmission in populations (Borchering et al 2017;Sage et al 2019). To counter these effects, organisms might show strong avoidance to scavenging of infected carcasses.…”